Hibernating Little Brown Myotis (Myotis lucifugus) Show Variable Immunological Responses to White-Nose Syndrome

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Moore, Marianne S ^a,b   Reichard, Jonathan D ^a,c   Murtha, Timothy D ^a,d   Nabhan, Morgan L ^a,e   Pian, Rachel E ^a,f   Ferreira, Jennifer S ^a,g   Kunz, Thomas H ^a  

^a USA   (United States)

^b BUCKNELL UNIVERSITY   (United States)

^c US Fish & Wildlife Service Massachusetts   (United States)

^d TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

^f ALBANY MEDICAL COLLEGE   (United States)

^g UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; IMMUNOGLOBULIN; INTERLEUKIN 4;

ANTIOXIDANT ACTIVITY; ARTICLE; B LYMPHOCYTE ACTIVATION; BAT; BLOOD SMEAR; CELL DIFFERENTIATION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FUNGUS; GEOMYCES DESTRUCTANS; HEMATOCRIT; HIBERNATION; HISTOPATHOLOGY; IMMUNE RESPONSE; LEUKOCYTE COUNT; MAMMALIAN DISEASE; MORBIDITY; MORTALITY; MYCOSIS; MYOTIS LUCIFUGUS; NONHUMAN; THERMOREGULATION; WHITE NOSE SYNDROME; WINTER;

ANIMAL DISEASES; ANIMALS; ASCOMYCOTA; CHIROPTERA; CYTOKINES; FEMALE; HIBERNATION; IMMUNOGLOBULINS; LEUKOCYTE COUNT; MYCOSES; SEASONS; UNITED STATES;

EID: 84875153041     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0058976     Document Type: Article

References (69)

1. Blehert DS, Hicks AC, Behr M, Meteyer CU, Berlowski-Zier BM, et al. (2009) Bat white-nose syndrome: an emerging fungal pathogen? Science 323: 227.
2. United States Fish and Wildlife Service (2012) News Release: North American bat death toll exceeds 5.5 million from white-nose syndrome. http//www.fws.gov/whitenosesyndrome/pdf/WNS_Mortality_2012_NR_FINAL.pdf. Accessed 4 May 2012.
3. Frick WF, Pollock JF, Hicks AC, Langwig KE, Reynolds DS, et al. (2010) An emerging disease causes regional population collapse of a common North American bat species. Science 329: 679-682.
4. Langwig KE, Frick WF, Bried JT, Hicks AC, Kunz TH, et al. (2012) Sociality, density-dependence and microclimates determine the persistence of populations suffering from a novel fungal disease, white-nose syndrome. Ecology Letters 15: 1050-1057.
5. Courtin F, Stone WB, Risatti G, Gilbert K, Van Kruiningen HJ, (2010) Pathogenic findings and liver elements in hibernating bats with white-nose syndrome. Veterinary Pathology 47: 214-219.
6. Meteyer CU, Buckles EL, Blehert DS, Hicks AC, Green DE, et al. (2009) Histopathologic criteria to confirm white-nose syndrome in bats. Journal of Veterinary Diagnostic Investigation 21: 411-414.
7. Warneke L, Turner JM, Bollinger TK, Lorch JM, Misra V, et al. (2012) Inoculation of bats with European Geomyces destructans supports the novel pathogen hypothesis for the origin of white-nose syndrome. Proceedings of the National Academy of Science 109: 6999-7003.
8. Reeder DM, Frank CL, Turner GG, Meteyer CU, Kurta A, et al. (2012) Frequent arousal from hibernation linked to severity of infection and mortality in bats with white-nose syndrome. PLoS One 7(6): e38920 doi:38910.31371/journal.pone.0038920.
9. Reichard JD, Kunz TH, (2009) White-nose syndrome inflicts lasting injuries to the wings of little brown myotis (Myotis lucifugus). Acta Chiropterologica 11: 457-464.
10. Fuller NW, Reichard JD, Nabhan ML, Fellows SR, Pepin LC, et al. (2011) Free-ranging little brown myotis (Myotis lucifugs) heal from wing damage associated with white-nose syndrome EcoHealth. 8: 154-162.
11. Gargas A, Trest MT, Christensen M, Volk TJ, Blehert DS, (2009) Geomyces destructans sp. nov. associated with bat white-nose sydrome. Mycotaxon 108: 147-154.
12. Lorch JM, Meteyer CU, Behr MJ, Boyles JG, Cryan PM, et al. (2011) Experimental infection of bats with Geomyces destructans causes white-nose syndrome. Nature doi:10.1038/nature10590.
13. Turner GG, Reeder DM, (2009) Update of white-nose syndrome in bats, September 2009. Bat Research News 50: 47-53.
14. Barbour RW, Davis WH (1969) Bats of America. Lexington: University of Kentucky Press.
15. Puechmaille SJ, Verdeyroux P, Fuller H, Gouilh MA, Bekaert M, et al. (2010) White-nose syndrome fungus (Geomyces destructans) in bat, France. Emerging Infectious Diseases 16: 290-293.
16. Wibbelt G, Kurth A, Hellmann D, Weishaar M, Barlow A, et al. (2010) White-nose syndrome fungus (Geomyces destructans) in bats, Europe. Emerging Infectious Diseases 16: 1237-1242.
17. Martínková N, Bačkor P, Bartonička T, Blažková P, Červený J, et al. (2010) Increasing incidence of Geomyces destructans fungus in bats from the Czeh Republic and Slovakia. PLoS ONE 5: e13853 doi:13810.11371/journal.pone.0013853.
18. Puechmaille SJ, Wibbelt G, Korn V, Fuller H, Forget F, et al. (2011) Pan-European distribution of white-nose syndrome fungus (Geomyces destructans) not associated with mass mortality. PLoS One 6(4): e19167 doi:19110.11371/journal.pone.0019167.
19. Pikula J, Bandouchova H, Novotny L, Meteyer CU, Zukal J, et al. (2012) Histopathology confirms white-nose syndrome in bats in Europe. Journal of Wildlife Diseases 48: 207-211.
20. Allen LC, Turmelle AS, Mendonça MT, Navara KJ, Kunz TH, et al. (2009) Roosting ecology and variation in adaptive and innate immune system function in the Brazilian free-tailed bat (Tadarida brasiliensis). Journal of Comparative Physiology B 179: 315-323.
21. Butler JE, Wertz N, Zhao Y, Zhang S, Bao Y, et al. (2011) The two suborders of chiropterans have the canonical heavy-chain immunoglobulin (Ig) gene repertoire of eutherian mammals. Developmental and Comparative Immunology 35: 273-284.
22. Bratch S, Wertz N, Chaloner K, Kunz TH, Butler JE, (2011) The little brown bat, M. lucifugus, displays a highly diverse VH, DH, and JH repertoire but little evidence of somatic hypermutation. Developmental and Comparative Immunology 35: 421-430.
23. Kepler TB, Sample C, Hudak K, Roach J, Haines A, et al. (2012) Chiropteran types I and II interferon genes inferred from genome sequencing traces by a statistical gene-family assembler. BMC Genomics 11: 444.
24. Hatten BA, Allen R, Sulkin SE, (1968) Immune response in Chiroptera to bacteriophage φX174. The Journal of Immunology 101: 141-150.
25. Hatten BA, Allen R, Sulkin SE, (1970) Studies on the immune capabilities of Chiroptera: I. Quantitative and qualitative nature of the immune responses in bats to bacteriophage φX174. The Journal of Immunology 105: 872-878.
26. Turmelle AS, Jackson FR, Green D, Mc Cracken GF, Rupprecht CE, (2010) Host immunity to repeated rabies virus infection in big brown bats. Journal of General Virology 91: 2360-2366.
27. Sulkin SE, Allen R, (1974) Virus infections in bats. Monographs in Virology 8: 1-103.
28. Tesh RB, Schneidau Jr JD, (1966) Experimental infection of North American insectivorous bats (Tadarida brasiliensis) with Histoplasma capsulatum. American Journal of Tropical Medicine and Hygiene 15: 544-551.
29. Greer DL, McMurray DN, (1981) Pathogenesis of experimental histoplasmosis in the bat, Artibeus lituratus. American Journal of Tropical Medicine and Hygiene 30: 653-659.
30. Turmelle AS, Ellison JA, Mendonça MT, McCracken GF, (2010) Histological assessment of cellular immune response to the phytohemagglutinin skin test in Brazilian free-tailed bats (Tadarida brasiliensis). Journal of Comparative Physiology B 180: 1155-1164.
31. Kupper TS, Fuhlbrigge RC, (2004) Immune surveillance in the skin: mechanisms and clinical consequences. Nature Reviews Immunology 4: 211-222.
32. Speth C, Rambuch G, Würzner R, Lass-Flörl C, (2008) Complement and fungal pathogens: an update. Mycoses 51: 477-496.
33. Takeda K, Kaisho T, Akira S, (2003) Toll-like receptors. Annual Reviews of Immunology 21: 335-376.
34. Romani L, (2011) Immunity to fungal infections. Nature Reviews 11: 275-288.
35. Shoham S, Levitz SM, (2005) The immune response to fungal infections. British Journal of Haematology 129: 569-582.
36. Moore MS, Reichard JD, Murtha TD, Zahedi B, Fallier RM, et al. (2011) Specific alterations in complement protein activity of little brown myotis (Myotis lucifugus) hibernating in white-nose syndrome affected sites. PLoS One 6(11): e27430 doi:27410.21371/journal.pone.0027430.
37. McMurray DN, Greer DL, (1979) Immune responses in bats following intranasal infection with Histoplasma capsulatum. American Journal of Tropical Medicine and Hygiene 28: 1036-1039.
38. Carey HV, Andrews MT, Martin SL, (2003) Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature. Physiological Reviews 83: 1153-1181.
39. Bouma HR, Carey HV, Kroese FGM, (2010) Hibernation: the immune system at rest? Journal of Leukocyte Biology 88: 619-624.
40. Jaeger R, (1963) Serologisch-hämatologische und immunologische Untersuchungen an winterschlafenden Fledermäusen (Myotis myotis). Experientia 19: 596-598.
41. Krutzsch PH, Hughes AH, (1959) Hematological changes with torpor in the bat. Journal of Mammalogy 40: 547-554.
42. Geiser F, Drury RL, Körtner G, Turbill C, Pavey CR, et al. (2004) Passive rewarming from torpor in mammals and birds: energetic, ecological and evolutionary implications. In: Barnes BM, Carey HV, editors. Life in the cold: evolution, mechanisms, adaptation, and application. Fairbanks, Alaska: Institute of Arctic Biology, University of Alaska Fairbanks. 209-219.
43. Kotts CE, White ME, Allen CE, Martin F, Dayton WR, (1987) A statistically standardized muscle cell culture bioassay measuring the effect of swine serum on muscle cell proliferation. Journal of Animal Science 64: 615-622.
44. Apak R, Güçlü K, Özyürek M, Karademir SE, (2004) Novel total antioxidant capacity index for dietary polyphenols and vitamins C and E, using their cupric ion reducing capability in the presence of neocuproine: CUPRAC method. Journal of Agricultural and Food Chemistry 52: 7970-7981.
45. Ono J, Yoshimura H, (2008) Prevention of hemaglobin interference of the formazan reaction. Clinica Chimica Acta 390: 115-121.
46. Jain NC (1993) Essentials of Veterinary Hematology. Philadelphia: Blackwell Publishing.
47. Bertrand S, Criscuolo F, Faivre B, Sorci G, (2006) Immune activation increases susceptibility to oxidative tissue damage in zebra finches. Functional Ecology 20: 1022-1027.
48. Sorci G, Faivre B, (2009) Inflammation and oxidative stress in vertebrate host-parasite systems. Philosophical Transactions of the Royal Society B Biological Sciences 364: 71-83.
49. Turner GG, Reeder DM, Coleman JTH, (2011) A five-year assessment of mortality and geographic spread of white-nose syndrome in North American bats and a look to the future. Bat Research News 52: 13-27.
50. Bouma HR, Strijkstra AM, Boerema AS, Deelman LE, Epema AH, et al. (2010) Blood cell dynamics during hibernation in the European Ground Squirrel. Veterinary Immunology and Immunopathology 136: 319-323.
51. Brack VJ, Twente JW, (1985) The duration of the period of hibernation of three species of vespertilionid bats. I. Field studies. Canadian Journal of Zoology 63: 2952-2954.
52. Casadevall A, (1995) Antibody immunity and invasive fungal infections. Infection and Immunity 63: 4211-4218.
53. Polonelli L, Casadevall A, Han Y, Bernardis F, Kirkland TN, et al. (2000) The efficacy of acquired humoral and cellular immunity in the prevention and therapy of experimental fungal infections. Medical Mycology 38: 281-292.
54. Ashman RB, Papdimitriou JM, (1993) Strain dependence of antibody-mediated protection in murine systemic candidiasis. Journal of Infectious Diseases 168: 511-513.
55. Dahlgren C, Karlsson A, (1999) Respiratory burst in human neutrophils. Journal of Immunological Methods 232: 3-14.
56. Kelly SA, Havrilla CM, Brady TC, Abramo KH, Levin ED, (1998) Oxidative stress in toxicology: established mammalian and emerging piscine model systems Environmental Health Perspectives. 106: 375-384.
57. Fridovich I, (1995) Superoxide radical and superoxide dismutases. Annual Review of Biochemistry 64: 97-112.
58. Peterhans E, (1997) Oxidants and antioxidants in viral diseases: disease mechanisms and metabolic regulation. Journal of Nutrition 127: 962S-965S.
59. Gharib B, Abdallahi OMS, Dessein H, Reggi MD, (1999) Development of eosinophil peroxidase activity and concomitant alteration of the antioxidant defenses in the liver of mice infected with Schistosoma mansoni. Journal of Hepatology 30: 594-602.
60. Postma NS, Mommers EC, Eling WM, Zuidema J, (1996) Oxidative stress in malaria: implications for prevention and therapy. Pharmacy World and Science 18: 121-129.
61. Ihara Y, Chuda M, Kuroda S, Hayabara T, (1999) Hydroxyl radical and superoxide dismutase in blood of patients with Parkinson's disease: relationship to clinical data. Journal of the Neurological Sciences 170: 90-95.
62. Metnitz PGH, Bartens C, Fischer M, Fridrich P, Steltzer H, et al. (1999) Antioxidant status in patients with acute respiratory distress syndrome. Intensive Care Medicine 25: 180-185.
63. Valentine JS, Doucette PA, Potter SZ, (2005) Copper-zinc superoxide dismutase and amyotrophic lateral sclerosis. Annual Reviews of Biochemistry 74: 563-593.
64. Monaghan P, Metcalfe NB, Torres R, (2009) Oxidative stress as a mediator of life history trade-offs: mechanisms, measurement, and interpretation. Ecology Letters 12: 75-92.
65. Lyman CP (1970) Thermoregulation and metabolism in bats. In: Wimsatt WA, editor. Biology of Bats. New York: Academic Press. 301-330.
66. Lopez-Torres M, Perez-Ocampo R, Barja de Quiroga G, (1991) Aging in brown fat: antioxidant defenses and oxidative stress. Mechanisms of Ageing and Development 59: 129-137.
67. Halliwell B, Chirico S, (1993) Lipid peroxidation: its mechanism, measurement, and significance. The American Journal of Clinical Nutrition 57: 715S-725S.
68. Tøien Ø, Drew KL, Chao ML, Rice ME, (2001) Ascorbate dynamics and oxygen consumption during arousal from hibernation in Arctic ground squirrels. American Journal of Physiology- Regulatory, Integrative and Comparative Physiology 281: R572-R583.
69. Kindt TJ, Goldsby RA, Osborne BA (2007) Kuby Immunology. New York: WH Freeman and Company.